Croaks

Croaking Science: Novel reproductive behaviours in amphibians

April 30, 2019 by editor

There are currently 8,004 species of amphibian (AmphibiaWeb, 2019) of which 88%, (7,064 species) are frogs and toads (anurans). These species exhibit an astonishing range of reproductive modes, of which only a small proportion lay eggs in water which hatch into aquatic larvae. In total, anurans exhibit 40 different modes of reproduction which are based on where the eggs are laid, egg type, and patterns of larval development. Examples of different reproductive modes include: depositing eggs in foam nests which float on water; laying eggs on the back of the female; laying eggs on the ground or in burrows; and depositing eggs on leaves with tadpoles that hatch and fall into water below (Duellman & Trueb, 1986). Of the 40 modes, direct developing embryos are perhaps the most unusual for amphibians. In these species, no water is required for development and instead the tadpoles develop within eggs which then hatch directly into froglets. This type of reproduction has evolved multiple times independently in anurans and currently 1,400 species are recognised to develop in this way (Stuart et al., 2008). Our knowledge of the full range of reproductive modes is still lacking as new patterns of reproduction are still being discovered. For example, some recent discoveries include novel nest building behaviour in the Kumbara night frog (Nyctibatrachus kumbara) from southern India (Gururaja et al., 2014) and unique foot-flagging behaviour has been observed in the Wayanad dancing frog (Micrixalus saxicola) a small torrent frog from India (Preininger et al., 2013). In this article we discuss some further recent discoveries of novel reproductive behaviours in anurans.

The Western Gnats in southern India has been a recent hotspot in discoveries of novel reproductive behaviours in anurans. Due to its glacial history and diversity of habitats, this region supports over 180 species of amphibian which exhibit a range of reproductive patterns. The Chalazodes bubble nest frog (Raorchestes chalazodes) inhabits remote tropical forests in the Western Gnats. This species was presumed to be extinct, until its recent rediscovery in 2011 (Ganesan et al., 2019). Sheshadri et al. (2015), have recently reported a unique breeding behaviour in this frog. Males were found living inside the shafts of bamboo canes where they guarded the eggs laid by the females (Figure 1). It appears that small holes created by insects in the lower shafts of bamboo canes are utilised by this frog, which uses the hollow interior for breeding. Males call to attract females, which lay 5-8 large eggs in clusters inside the bamboo. The male guards these eggs from predators until they hatch into free-living froglets. This is the first time that this type of reproduction has been recorded in any amphibian species and thus represents a unique reproductive mode (Sheshadri et al., 2015). Unfortunately, this frog remains critically endangered, only occurring in five localities, and is highly threatened due to over-harvesting of bamboo (Sheshadri et al., 2015). Unless unregulated overharvest of bamboo is halted, this species may well go extinct due to lack of suitable breeding habitat.Figure 1. Left: Adult Chalazodes bubble nest frog (Raorchestes chalazodes) on top of a bamboo cane; Right: cross section of bamboo cane showing clutch of eggs and an emerging froglet.

***Figure 1.*** *Left: Adult Chalazodes bubble nest frog* (Raorchestes chalazodes) *on top of a bamboo cane; Right: cross section of bamboo cane showing clutch of eggs and an emerging froglet.* [Photo credit: Sheshadri et al., 2015]

Many species of male anuran possess vocal sacs which they use during breeding to vocalise to attract females. In several frog species visual cues of the inflating vocal sac make the acoustic signal more attractive to females or aid to deter competing males. Male African reed frogs (Hyperoliidae) possess a prominent gular patch on the vocal sac which they use to attract females and may also function as a visual cue to competing males (Figure 2). Starnberger et al. (2018) found that in the spotted reed frogs (Hyperolius puncticulatus) males do not respond to the vocal sac of other males but when they heard males calling they performed a previously undescribed gestural display: a tapping behaviour consisting of a series of front and hind limb lifts. It is thought that these gestures serve to deter males and also attract females who may be close by (Starnberger et al., 2018).F

***Figure 2.*** *Male spotted reed frogs (*Hyperolius) often have conspicuous vocal sacs which they use to vocalise and attract females. [Photo credit: Luke & Ursula Verburgt, http://africanamphibians.myspecies.info/file-colorboxed/8072]

Many anurans form amplexus during breeding where by the male takes the female in an embrace. Since fertilization is external in most anurans, the position of the male ensures that he is able to release his sperm to fertilize her eggs as she releases them. The night frogs (genus Nyctibatrachus) from India contains 28 species, many of which have only recently been described. In all Nyctibatrachus species, egg clutches are deposited on rocks or vegetation overhanging water, and tadpoles fall in the water after hatching, where they continue their development. Several novel types of amplexus have been described in this genus (reviewed in Willaert et al., 2016) such as a short axillary amplexus in pairs of the Kumbara night frog (N. kumbara) followed by a handstand, or the complete absence of amplexus in N. petraeus where the female deposits her eggs prior to the male fertilizing them. Willaert et al. (2016) have recently discovered a new breeding behaviour in the Bombay night frog (N. humayuni). During breeding the male forms a loose amplexus on the female, lasting only a few seconds and differs from all previously described amplexus types in anurans. When mounted, the male rests on the female without grabbing her tightly, but instead uses his hands to hold on to a leaf, branch or tree trunk (Willaert et al., 2016). Since the male does not have time to fertilise the eggs whilst engaged with the female, the authors propose that the male releases his sperm onto the back of the female and the eggs are subsequently fertilized by the sperm running down her back and hind legs. This hypothesis is supported by the observation that the female remains motionless after egg deposition for several minutes with her hind legs stretched around the freshly deposited clutch (Willaert et al., 2016) (Figure 3). In addition, females have been observed to make a call which is highly unusual. Female calling behaviour has so far only been reported in only 25 anurans, representing less than 0.5% of the total anuran species that are currently recognized (Willaert et al., 2016). It appears that the females call to aid in mate recognition and location.

***Figure 3.*** *A female Bombay night frog (*N. humayuni) *deposits hers eggs and remains motionless with her hind legs stretched around the eggs. The male is sitting close-by without any physical contact with the* female. [*Photo credit: Willaert et al., 2016]*

This study, along with others recently published, demonstrate the range of reproductive behaviours that are exhibited amongst anurans. The Nyctibatrachus frogs are one of several unique taxa in the Western Ghats biodiversity hotspot and are heavily threatened by human activities. Understanding the ecology of these and other poorly known species is of major importance for planning and successfully implementing conservation strategies.

References

AmphibiaWeb (2019). <https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 18 Apr 2019.

Duellman, W.E. & Trueb, L. (1986) Biology of Amphibians, McGraw-Hill Publishing Company, United States of America.

Ganesan, R., Seshadri, K.S. & Biju, S.D. (2019) Lost! Amphibians of India. Available at: http://www.lostspeciesindia.org/LAI2/new1_rediscovered.php. Accessed 18 April 2019.

Gururaja, K.V., Dinesh, K.P., Priti, H. & Ravikanth, G. (2014) Mud- packing frog: a novel breeding behaviour and parental care in a stream dwelling new species of Nyctibatrachus (Amphibia, Anura, Nyctibatrachus). Zootaxa, 3796: 33-61.

Preininger, D., Boeckle, M., Freudmann, A., Starnberger, I., Sztatecsny, M. & Hödl M. (2013) Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment. Behavioral Ecology and Sociobiology, 67: 1449–1456.

Seshadri, K.S., Gururaja, K.V. & Bickford, D.P. (2015) Breeding in bamboo: a novel anuran reproductive strategy discovered in Rhacophorid frogs of the Western Ghats, India. Biological Journal of the Linnean Society, 14 (1): 1-11. https://doi.org/10.1111/bij.12388

Starnberger, I., Maier, P.M., Hödl, W. & Preininger, D. (2018) Multimodal signal testing reveals gestural tapping behavior in spotted reed frogs. Herpetologica, 74 (2): 127–134.

Stuart, S.N., Hoffmann, M., Chanson, J.S., Cox, N.A., Berridge, R.J., Ramani, P. & Young, B.E. (2008) Threatened Amphibians of the World. Barcelona, Spain: Lynx Edicions; Gland, Switzerland: IUCN, Arlington, Virginia, USA: Conservation International.

Willaert, B., Suyesh, R., Garg, S., Giri, V.B., Bee, M.A. & Biju, S.D. (2016) A unique mating strategy without physical contact during fertilization in Bombay Night Frogs (Nyctibatrachus humayuni) with the description of a new form of amplexus and female call. PeerJ 4:e2117; DOI 10.7717/peerj.2117

CJ Wildlife – Your Spring Offer!

January 31, 2019 by editor

This month, CJ Wildlife – Europe’s leading garden wildlife specialist and Froglife partner are reminding us that all of our gardens, no matter what size, can become bustling nature reserves for our local wildlife, so the more species you can cater for – from the smallest insect to the largest toad – the more alive your garden will become this spring.

We’re now in the last full month of winter and, whatever February throws at us, spring isn’t too far away. Hedgehogs and bats should still be hibernating, but the first squirrel litters are likely to be born anytime and, by the end of the month, an increasing number of ponds will have frog spawn.

Birds will be looking for nesting territories, which makes February the ideal month to put up a new nest box and keeping feeders topped up will ensure birds know they can rely on your garden for a reliable source of food, vital when choosing somewhere to raise their young.

For hints and tips on making the perfect wildlife garden this spring, visit www.birdfood.co.uk, plus as a Froglife supporter, you can save 10% off when you buy from CJ Wildlife, simply use discount code UKFROG18 when you order.

What our Animals are doing this month…

January 31, 2019 by editor

What our animals are doing this month…. February 2019 Edition

It’s probably not quite hot enough for many of our amphibians to get back into the swing of things, but by mid to late February it’s likely some amphibians will be moving back to ponds and for our common frog even breeding / laying frogspawn.

Smooth newts may have made their way back to ponds within the month of February after traversing some difficult terrain on their travels from overwintering areas to a pond. But how do they make this journey through what may be areas of tall, dense vegetation back to their breeding pond? The majority of amphibians return to the same pond year after year – hence they must have some form of navigation. For smooth newt and great crested newt, they use their sense of smell to navigate back to the pond as well as the calls of common toad. However, if smooth or great crested newts are displaced away from their home range – their sense of smell and hearing won’t be adequate to navigate back to their preferred pond.

The palmate newt has displayed an additional method of navigation however using a sense called magnetoreception. This sense acts a geomagnetic compass the palmate newt can use to find its way back to its breeding pond, even if displaced up to 19km outside of its range.

*Smooth newts can reach their breeding pond as early as February after some nifty navigation. Photo credit – Gareth Ward*

Croaking Science: Caecilians – unusual reproductive ecology

November 29, 2018 by editor

Croaking Science: Caecilians – unusual reproductive ecology

Caecilians, or blind snakes, as they are also often called, are limbless, elongate amphibians which inhabit tropical regions, with hotspots in South America and Asia (Kupfer et al., 2016; Gomes et al., 2012). Of all the groups of amphibians, caecilians are the most poorly understood, which is in part due to their secretive, fossorial lifestyle (Figure 1). They belong to the order Gymnophiona, one of three orders which comprises the Amphibia. There are currently 209 recognised species, which represents just 3% of the total 7,950 amphibian species worldwide (AmphibiaWeb, 2018). Caecilians are all ground-dwelling tropical amphibians which exhibit a wide range of reproductive modes, from laying eggs which hatch into aquatic larvae to those which hatch into miniature terrestrial juveniles. Little is known of their diverse reproductive modes but in recent years research has elucidated more information on their unusual breeding ecology.

**Figure 1.** Caecilians have an unusual appearance, being primarily fossorial and elongate in form. *[Photo credit: Will Brown – Brown-snouted Blind Snake (Ramphotyphlops wiedii or nirgrogrescens) 3, CC BY 2.0,https://commons.wikimedia.org/w/index.php?curid=71399151]*

Oviparous caecilians lay eggs, which are usually laid in a small terrestrial nest (Figure 2). The females of all these species exhibit extensive parental care, guarding their clutches of eggs against predators (Gomes et al., 2012). Eggs will hatch into either free-swimming larvae which develop in small water bodies, or terrestrial juveniles which are independent of their parents. Ichthyophis kohtaoensis inhabits the tropical forests of northern Thailand and belongs to the second largest caecilian family. In this species, breeding coincides with the rainy season with clutches of eggs laid in damp soil at the onset of the first rains (Kupfer et al., 2004). Females lay their eggs in small chambers near to temporary and permanent ponds, pools and slow flowing brooks and rivers. This allows the free-swimming larvae to readily hatch into the water to complete their aquatic development. Research suggests that females eat little or no food during the three month incubation period since the body condition of females attending young clutches is higher than those with older clutches (Kupfer et al., 2004). This, along with the small clutch size, indicates that there are costs to parental investment and attending eggs. In addition, there is a correlation between female body length and clutch size with older females being longer than young females (Kupfer et al., 2004). This implies that older, more experienced females produce larger clutches and more offspring (Kupfer et al., 2004).

**Figure 2.** A female caecilian guarding her brood of eggs from predators. *[Photo credit: Davidvraju, Creative Commons Attribution-Share Alike 4.0 International, https://commons.wikimedia.org/wiki/File:Caecilian_guarding_its_eggs.jpg]*

The ringed caecilian, Siphonops annulatus, is an unusual oviparous species inhabiting South America. The eggs hatch into poorly developed terrestrial young which feed on the skin of the female. The young possess specialised teeth which allow them to scrape skin from their mother’s back immediately after hatching (Wilkinson et al., 2008). The feeding behaviour of the young is described as being “quite frenetic with the young frequently tearing pieces of skin by spinning along their long axes and sometimes struggling over the same piece of skin” (Wilkinson et al., 2008) (Figure 3). This maternal dermatophagy is also known from a second, distantly related African caecilian species, Boulengerula taitana (Kupfer et al., 2008), which suggests that skin feeding is an ancient form of caecilian parental care and may have persisted for more than 100 million years (Wilkinson et al., 2008). In addition, Wilkinson et al. (2008) report a previously undocumented behaviour which involves the female raising herself upward, exposing her vent and releasing a clear fluid, which the young consume. This appears to be a form of feeding the young, but further studies are required to ascertain the function of this behaviour.

**Figure 3.** A caecilian mother with eggs which will hatch into young which feed off her skin. *[Photo credit: Wilkinson M, Sherratt E, Starace F, Gower DJ (2013)]*

Viviparous caecilians, which give birth to live young, represent another unusual reproductive mode for amphibians. During development inside the female, the foetuses initially obtain their nutrition from a yolk, similar to egg-developing species. After this, the developing young feed on a uterine milk, secreted from the oviducts of the female. The young obtain this through possessing specialised embryonic teeth which they use to scrape at the oviduct wall (Gomes et al., 2012). The evolution of viviparity in caecilians is poorly understood, but since both viviparous and oviparous species possess specialised teeth for scraping (either skin or oviduct milk), this suggests that all these species evolved from a common, oviparous ancestor (Kupfer et al., 2006). Gegeneophis seshachari is the only known species of viviparous caecilian from the Indo-Seychellean region (Gower et al., 2008). In this area the rainy season is short and unpredictable such that laying eggs which hatch into offspring that rely on the presence of water or a damp environment may be highly risky. Water bodies may dry up rapidly before larvae can fully develop. Therefore, Gower et al. (2008) propose that viviparity may have evolved in this species in response to short, unpredictable rainy seasons and the lack of suitable locations to lay and incubate their eggs.

Caecilians possess interesting and unusual reproductive modes, much of which is poorly understood. In addition, many of these species are threatened or Data Deficient and in regions which are undergoing large habitat loss and fragmentation. More primary data are required to fully understand caecilian reproductive ecology and evolution, which will help inform much needed improvements in conservation assessments for these species.

References

AmphibiaWeb (2018) https://amphibiaweb.org. University of California, Berkeley, CA, USA. Accessed 15 Nov 2018.

Gomes, A.D., Moreira, R.G., Navas, C.A., Antoniazzi, M.M. and Jared, C. (2012). Review of the reproductive biology of caecilians (Amphibia, Gymnophiona). South American Journal of Herpetology, 7 (3): 191-202.

Gower, D.J., Giri, V., Dharne, M.S. and Shouche, Y.S. (2008) Frequency of independent origins of viviparity among caecilians (Gymnophiona): evidence from the first ‘live-bearing’ Asian amphibian. Journal of Evolutionary Biology, 21: 1220–1226.

Kupfer, A.K., Nabhitabhata, J. and Himstedt, W. (2004) Reproductive ecology of female caecilian amphibians (genus Ichthyophis): a baseline study. Biological Journal of the Linnean Society, 83: 207-217.

Kupfer, A., Müller, H., Antoniazzi, M.M., Jared, C., Greven, H., Nussbaum, R.A. and Wilkinson, M. (2006) Parental investment by skin feeding in a caecilian amphibian. Nature, 440 (13 April 2006), doi:10.1038/nature04403.

Kupfer, A., Wilkinson, M., Gower, D.J. Müller, H. and Jehle, R. (2008) Care and parentage in a skin-feeding caecilian amphibian. Journal of Experimental Biology, 309A: 460–467.

Kupfer, A., Maxwell, E., Reinhard, S. and Kuehnel, S. (2016) The evolution of parental investment in caecilian amphibians: a comparative approach. Biological Journal of the Linnean Society, 119: 4–14.

Wilkinson, M., Kupfer, A., Marques-Porto, R., Jeffkins, H., Antoniazi, M.M. and Jared, C. (2008) One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona). Biological Letters, 4: 358–361.

doi:10.1098/rsbl.2008.0217

Inspired By Nature: A Poem of Return

July 18, 2018 by editor

Inspired by Nature: A Poem of Return

Froglife’s Communications & Fundraising Officer, Ashlea Mawby, felt inspired by the work she does here at Froglife and wrote this poem.

Croaking Science: Kin Recognition

May 31, 2018 by editor

Kin recognition – when recognising relatives is important

During the spring in temperate countries tadpoles of frogs and toads often develop in a range of water bodies from small ponds to lakes. Swimming around in the open water, tadpoles are highly vulnerable to predation so in many species such as the common toad (Bufo bufo), tadpoles swim in large groups or shoals (Figure 1). By living in groups the tadpoles gain advantages such as decreased risks of predation and increased access to food. However, there are costs to group living such as an increase in the risk of transmitting infectious disease and intraspecific competition. Research has shown that tadpoles further increase the benefits of group living by associating with relatives, or close kin. If forming shoals reduces the risk of predation, then swimming with relatives who possess similar genes will increase the chances that these genes will survive to the next generation. The exact mechanism of kin recognition in anuran tadpoles is not clear but studies suggest that frog and toad tadpoles recognise each other through chemical cues (Eluvathingal et al., 2009). The persistent dense swimming shoals of tadpoles of many amphibians from the genera Rana and Bufo (e.g. wood frog (Rana sylvatica); common toad (Bufo bufo); and boreal toad (Bufo boreas)) have been shown to consist primarily of associations of closely related kin (Blaustein & Waldman, 1982). However, in the red-legged frog (Rana aurora), Schneider’s toad (Duttaphrynus scaber) and Günther’s golden-backed frog (Indosylvirana temporalis), tadpoles only exhibit kin recognition early in their development when they form dense shoals. As they mature, tadpoles disperse and kin recognition drops (Rajput et al., 2014). During late development the risks of pond desiccation are high and individual tadpoles seek isolated patches of water. Under these conditions the risks of suffocation through desiccating water is higher than the benefits of associating with relatives. Further to this, recent research has shown that the persistence of associating with kin varies considerably even within a single species. For example, larvae of the wood frog (Rana sylvatica) from North America exhibits kin recognition and individuals often choose to swim with relatives. However, Halverston et al. (2006) have shown that the level and occurrence of swimming with relatives is not consistent but depends on a range of factors including levels of competition, predation and parasitism. Tadpoles from two adjacent ponds exhibited different levels of association with kin due to localised differences in these factors (Halverston et al., 2006). This demonstrates that associating and swimming with relatives only occurs under certain environmental conditions and groups of tadpoles may show variations in their degree of kin association.

*Figure 1. Several species of Bufo tadpole form shoals which may consist of close relatives.*

Many amphibians within temperate zones are herbivorous, however there are a number of tropical species of tadpole which are carnivorous. This provides the opportunity for cannibalism to evolve where larger tadpoles may predate smaller ones within the same species. In these species it may be advantageous for tadpoles to recognise kin to avoid potential predation on relatives who carry the same genes. Research has shown that cannibalism generally occurs when the nutritional benefits gained from eating relatives outweigh the disadvantages such as risks of injury, transmitting infectious diseases and losing potential members of the same species who carry similar genes. As a result, cannibalism has evolved in some carnivorous amphibian larval species, but not others, depending on the environmental conditions and the relative advantages and disadvantages of consuming close kin.

Many tropical frogs in the genus Dendrobates lay their eggs in terrestrial habitats that are then transported by males to small water-filled water bodies formed in the axils of tree leaves (phytotelmata). Females of the poison dart frog Dendrobates auratus only lays a few eggs per year, so the number of tadpoles developing within any given water body is low. In some species of Dendrobates frogs, the female lays non-fertile eggs into the water to feed the tadpoles. However, female D. auratus does not perform this behaviour so the tadpoles rely completely on external food sources e.g. fallen insects, for survival. Starvation within such small water bodies is very high and therefore cannibalism has evolved to allow some of the tadpoles to survive. In this species the larger tadpoles predate the smaller ones which provides additional nutrition which is crucial for survival. However, male D. auratus may bring tadpoles from a number of clutches so there is also the potential for kin recognition i.e. larger tadpoles may choose to consume non-relatives over relatives since the latter may share the same genes. However, experiments carried out by Gray et al. (2009) suggest this is not the case and that larger tadpoles indiscriminately predate kin from non-kin. The authors hypothesise that since food sources are so scarce for developing tadpoles then the benefits of individual survival outweigh the costs of losing genetic relatives.

Additional research by Poelman & Dicke (2007) has shown that in the poison dart frog Ranitomeya ventrimaculata, females exhibit a plasticity in where she lays her eggs, which depends on environmental conditions (Figure 2). In this species, like D. auratus, tadpoles are highly cannibalistic, consuming both kin and non-kin. At the beginning of the breeding season, when water-filled phytotelmata do not contain many tadpoles, the female will spread her eggs widely amongst different water bodies, avoiding those which already contain a tadpole. This reduces the chances that her eggs will get consumed by another tadpole (which may or may not be her own). However, nearer to the end of the breeding season, the female changes behaviour and actively starts laying more eggs in phytotelmata which already contain large tadpoles. Poelman & Dicke (2009) hypothesise that this is because at the end of the breeding season there are few free phytotelmata left and by provisioning those that already contain tadpoles with fertilised eggs, she is providing food to the tadpoles which may be her own. This sacrifice of eggs will indirectly improve the survival of her existing tadpoles, the eggs of which she laid early in the breeding season. This plasticity in behavioural response allows a greater number of tadpoles to survive when the risk of desiccation of water bodies is high.

Figure 2. The poison dart frog Ranitomeya ventrimaculata exhibits different egg-laying strategies depending on the environmental conditions.

The green and golden bell frog (Litoria aurea) was once a common species widely distributed in south eastern Australia (Figure 3). It has also been introduced into New Zealand and surrounding islands. However, the extreme sensitivity of these species to the infectious chytrid fungus has been the major cause of the species’ decline in its native range and the species is currently restricted to small isolated populations. The tadpoles form groups where individuals gain protection from predators, increased foraging efficiency and better growth. Associating with relatives is advantageous since individuals would be indirectly protecting those carrying similar genes. Pizzatto et al. (2016) examined the behaviour of tadpoles of the green and golden bell frog in relation to kin recognition. The authors found that in the bell frog L. aurea tadpoles did indeed distinguish kin from non-kin and thus formed shoals containing mainly relatives. The authors suggest the advantages to this species include increased growth and increased resistance to disease since related members are likely to carry the same disease resistance genes.

Figure 3. Tadpoles of the green and golden bell frog (Litoria aurea) from Australia congregate in groups containing related individuals.

References

Blaustein, A.R. & Waldman, B. (1982) Kin recognition in anuran amphibians. Animal Behaviour, 44: 207 -221.

Eluvathingal, L.M., Shanbhag, B.A. & Saidapur, S.K. (2009) Association preference and mechanism of kin recognition in tadpoles of the toad Bufo melanostictus. Journal of Bioscience, 34 (3): 435–444.

Gray, H.M., Summers, K. & Ibáñez, R.D. (2009) Kin discrimination in cannibalistic tadpoles of the Green Poison Frog, Dendrobates auratus (Anura: Dendrobatidae). Phyllomedusa, 81 (1): 41-50.

Halverson, M.A., Skelly, D.K. & Caccone, A. (2006) Kin distribution of amphibian larvae in the wild. Molecular Ecology, 15: 1139–1145.

Poelman, E.H. & Dicke, M. (2007) Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evolution and Ecology, 21: 215–227.

Pizzatto, L., Stockwell, M., Clulow, S., Clulow, J. & Mahony, M. (2016) How to form a group: effects of heterospecifics, kinship and familiarity in the grouping preference of green and golden bell frog tadpoles. Journal of Herpetology, 26: 157–164.

Rajput, A.P., Saidapur, S.K. & Shanbhag, B.A. (2014) Kin discrimination in tadpoles of Hylarana

temporalis (Anura: Ranidae) and Sphaerotheca breviceps (Anura: Dicroglossidae): influence of hydroperiod and social habits. Phyllomedusa, 13 (2): 119–131.

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